Abstract
The brain of the bottlenose dolphin exhibits patterns of isocortical parcellation and cytoarchitecture distinct from those seen in primates, yet cell clusters in anterior insula are comparable in scale to module-like cell arrangements found throughout isocortex in other placental mammalian species with long divergent evolutionary histories. This similarity may be due to common ancestry, or to convergence as a result of selective constraints on organization of connections within such modules. Differences reflect alternate arrangements of minicolumns, an elemental cytoarchitectonic motif of isocortex defined by radially oriented pyramidal cell arrays. In contrast with larger modular structures incorporating them, minicolumns have been highly conserved in mammalian evolution. In this study a previously validated imaging method was employed to assess verticality, D, a parameter indicating radial bias of isocortex. Photomicrographs of coronal Nissl-stained sections of dolphin anterior insular cortex were compared with sections from human brains of putatively homologous areas as well as other isocortical areas differing in modular organization. Dolphin insula exhibited a high degree of verticality consistent with conserved minicolumnar organization. Our findings indicate that a basic structural motif of isocortex is synapomorphic in a species of marine mammal exhibiting unique phylogenetically derived isocortical characteristics.
[1] Kaas J.H., From mice to men: the evolution of the large, complex human brain, J. Biosci., 2005, 30, 155–165 http://dx.doi.org/10.1007/BF0270369510.1007/BF02703695Search in Google Scholar
[2] Marino L., Convergence in complex cognitive abilities in cetaceans and primates, Brain Behav. Evol., 2002, 59, 21–32 http://dx.doi.org/10.1159/00006373110.1159/000063731Search in Google Scholar
[3] Jerison H.J., Evolution of the brain and intelligence, Academic Press, New York, 1973 10.1016/B978-0-12-385250-2.50018-3Search in Google Scholar
[4] Northcutt R.G., Kaas J.H., The emergence and evolution of mammalian neocortex, Trends Neurosci., 1995, 18, 373–379 http://dx.doi.org/10.1016/0166-2236(95)93932-N10.1016/0166-2236(95)93932-NSearch in Google Scholar
[5] Kesarev V.S., Malofeeva L.I., Trykova O.V., Structural organization of the cerebral neocortex in cetaceans in cetaceans, Arh. Anat. Gistol. Embriol., 1977, 73, 23–30 Search in Google Scholar
[6] Morgane P.J., Jacobs M.S., McFarland W.L., The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus): surface configurations of the telencephalon of the bottlenose dolphin with comparative anatomical observations in four other cetacean species, Brain Res. Bull., 1980, 5(3 suppl. 1), 1–107 http://dx.doi.org/10.1016/0361-9230(80)90272-510.1016/0361-9230(80)90272-5Search in Google Scholar
[7] Manger P., Sum M., Szymanski M., Ridgeway S., Krubitzer L., Modular subdivisions of dolphin insular cortex: does evolutionary history repeat itself? J. Cogn. Neurosci., 1998, 10, 153–166 http://dx.doi.org/10.1162/08989299856262710.1162/089892998562627Search in Google Scholar
[8] Hof P.R., Chanis R., Marino L., Cortical complexity in cetacean brains, Anat. Rec. A Discov. Mol. Cell. Evol. Biol., 2005, 287, 1142–1152 10.1002/ar.a.20258Search in Google Scholar
[9] Hof P.R., Van der Gucht E., Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae), Anat. Rec., 2007, 290, 1–31 http://dx.doi.org/10.1002/ar.2040710.1002/ar.20407Search in Google Scholar
[10] Gressens P., Evrard P., The glial fascicle: an ontogenic and phylogenic unit guiding, supplying and distributing mammalian cortical neurons, Brain Res. Dev. Brain Res., 1993, 76, 272–277 http://dx.doi.org/10.1016/0165-3806(93)90218-Y10.1016/0165-3806(93)90218-YSearch in Google Scholar
[11] Buxhoeveden D.P., Casanova M.F., The minicolumn and evolution of the brain: a review, Brain Behav. Evol., 2002, 60, 125–151 http://dx.doi.org/10.1159/00006593510.1159/000065935Search in Google Scholar PubMed
[12] Mountcastle V.B., Introduction, Cereb. Cortex, 2003, 13, 2–4 http://dx.doi.org/10.1093/cercor/13.1.210.1093/cercor/13.1.2Search in Google Scholar
[13] Mountcastle V.B., An organizing principle for cerebral function: the unit module and the distributed system, In: Edelman G.M., Mountcastle V.B., The mindful brain: cortical organization and the group-selective theory of higher brain function, MIT Press, Cambridge, 1978, 7–51 Search in Google Scholar
[14] Casanova M.F., Trippe J., Switala A., A temporal continuity to the vertical organization of the human neocortex, Cereb. Cortex, 2007, 17, 130–137 http://dx.doi.org/10.1093/cercor/bhj13410.1093/cercor/bhj134Search in Google Scholar
[15] Rakic P., A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution, Trends Neurosci., 1995, 18, 383–388 http://dx.doi.org/10.1016/0166-2236(95)93934-P10.1016/0166-2236(95)93934-PSearch in Google Scholar
[16] Casanova M.F., Switala A.E., Minicolumnar morphometry: Computerized image analysis. In: Casanova M.F. (Ed.), Neocortical modularity and the cell minicolumn, Nova Science Publishers, New York, 2005, 165–184 Search in Google Scholar
[17] Casanova M.F., Switala A.E., Trippe J., A comparison study of the vertical bias of pyramidal cells in the hippocampus and neocortex, Dev. Neurosci., 2007, 29, 193–200 http://dx.doi.org/10.1159/00009622310.1159/000096223Search in Google Scholar PubMed
[18] Pourdeyhimi B., Xu B., Nayernouri A., Evaluating carpet appearance loss: pile lay orientation, Text. Res. J., 1994, 64, 130–135 http://dx.doi.org/10.1177/00405175940640030210.1177/004051759406400302Search in Google Scholar
[19] Buxhoveden D.P., Casanova M.F., Encephalization, minicolumns, and hominid evolution. In: Casanova M.F. (Ed.), Neocortical modularity and the cell minicolumn, Nova Science Publishers, New York, 2005, 119–138 Search in Google Scholar
[20] Krmpotić-Nemanić J., Kostović I., Nemanić Đ., Prenatal and perinatal development of radial cell columns in the human auditory cortex, Acta Oto-Laryngol., 1984, 97, 489–495 http://dx.doi.org/10.3109/0001648840913292610.3109/00016488409132926Search in Google Scholar PubMed
[21] Cherniak C., Component placement optimization in the brain, J. Neurosci., 1994, 14, 2418–2427 10.1523/JNEUROSCI.14-04-02418.1994Search in Google Scholar
[22] Kaas J.H., The evolution of isocortex, Brain Behav. Evol., 1995, 46, 187–196 http://dx.doi.org/10.1159/00011327310.1159/000113273Search in Google Scholar PubMed
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